Phage-host interactions as a driver of population dynamics during wine fermentation: Betting on underdogs

Winemaking is a complex process in which numerous microorganisms, mainly yeasts and lactic acid bacteria (LAB), play important roles. After alcoholic fermentation (AF), most wines undergo malolactic fermentation (MLF) to improve their organoleptic properties and microbiological stability. Oenococcus oeni is mainly responsible for this crucial process where L-malic acid (MA) in wine converts to softer L-lactic acid. The bacterium is better adapted to the limiting conditions imposed by the wine matrix and performs MLF under regular winemaking conditions, especially in wines with a pH below 3.5. Traditionally, this process has been conducted by the natural microbiota present within the winery. However, the start, duration and qualitative impact of spontaneous MLF are unpredictable, which prompts winemakers to use pure starter cultures of selected bacteria to promote a more reliable, simple, fast and efficient fermentation. Yet, their use does not always ensure a problem-free fermentation. Spontaneous initiation of the process may prove very difficult or does not occur at all. Such difficulties arise from a combination of factors found in some wines upon the completion of AF (high ethanol concentration, low temperature and pH, low nutrient concentrations, presence of free and bound SO₂). Alongside these well documented facts, research has also provided evidence that negative interactions between O. oeni and other biological entities such as yeasts may also impact MLF. Another insufficiently described, but highly significant factor inhibiting bacterial growth is connected to the presence of bacteriophages of O. oeni which are frequently associated to musts and wines. The purpose of this review is to summarize the current knowledge about the phage life cycles and possible impacts on the trajectory of the microbiota during winemaking.